FORUM
Drosophila suzukii in Southern Neotropical Region: Current Status and Future Perspectives
F A
NDREAZZA1, D B
ERNARDI2, RSS
DOSS
ANTOS3, FRM G
ARCIA4, EE O
LIVEIRA1, M B
OTTON3, DE N
AVA51Depto de Entomologia, Univ Federal de Viçosa, Viçosa, MG, Brasil
2Depto de Fitossanidade, Univ Federal de Pelotas, Capão do Leão, RS, Brasil
3Lab de Entomologia, Embrapa Uva e Vinho, Bento Gonçalves, RS, Brasil
4Programa de Pós-graduação em Entomologia, Instituto de Biologia, Univ Federal de Pelotas, Capão do Leão, RS, Brasil
5Lab de Entomologia, Embrapa Clima Temperado, Pelotas, RS, Brasil
Abstract Keywords
Spotted wing drosophila, area-wide integrated pest management, pest control, alien pest invasions
Correspondence
F Andreazza, Depto de Entomologia, Univ Federal de Viçosa, Av. Peter Henry Rolfs s/n 36570 - 900, Viçosa, MG, Brasil; felipe.
andreazza@ufv.br
Edited by Lessando Moreira Gontijo - UFV Received 24 April 2017 and accepted 7 August 2017
*Sociedade Entomológica do Brasil 2017
Non-native insect pests are often responsible for important damage to native and agricultural plant hosts. SinceDrosophila suzukiiMatsumura (Diptera: Drosophilidae) has become an important pest in North America and Europe (i.e., in 2008), the global production of soft thin-skinned fruits has faced severe production losses. In the southern Neotropical region, however, the first record ofD. suzukiioccurred in 2013 in the south of Brazil. It has also been recorded in Uruguay, Argentina, and Chile. Despite its recent occurrence in the southern Neotropical region, the fast disper- sion of D. suzukiihas inspired local research efforts in an attempt to mitigate the consequences of this insect pest invasion. In this forum, we explore the current status ofD. suzukiiin southern Neotropical regions, discussing its future perspectives. Additionally, we attempt to draft activ- ities and a research agenda that may help to mitigate the losses caused by D. suzukii in native and commercial soft-skinned fruits produced in this region. Currently,D. suzukiiappears to be well established in the south of Brazil, but considering the entire southern Neotropical region, the invasion panorama is still underinvestigated. The lack of studies and regulatory actions againstD. suzukiihas contributed to the invasion success of this species in this region. Considering several peculiarities of both the pest biology and the environmental of this region, the authors advocate for the need of intensive and integrative studies toward the development and implementation of area-wide integrated pest management programs againstD. suzukiiin the southern Neotropical region.
Introduction
Historically, alien pest invasions usually result in severe production losses due to economic, social, and health damage (Jackson & Lee 1985, Benedict et al 2007, Desneuxet al2011, Asplenet al2015, Kriticoset al2015, Singer2017). The final scenario for pest establishment as well as the number of necessary efforts to mitigate the environmental disturbances caused by the pest has been
a persistent question (Perringset al 2002, Desneuxet al 2011, Asplenet al2015). However, early studies predicting all possible aspects of local interactions of the alien species with known or other potential hosts, pest competitiveness with the native species and susceptibility to endemic nat- ural enemies can greatly aid the organization and devel- opment of the most adequate management plans (Cini et al 2012, Asplen et al 2015, Kriticos et al 2015). It is, however, worth noting that the use of current knowledge DOI 10.1007/s13744-017-0554-7
obtained in areas previously invaded by the alien pest will also help to organize and plan such efforts.
A l t h o u g h Z a p r i o n u s i n d i a n u s G u p t a ( D i p t e r a : Drosophilidae) has been well established as an important in- sect pest of the fig,Ficus caricaL. (Moraceae), in Brazil (Raga et al 2003), Drosophila suzukii Matsumura (Diptera:
Drosophilidae), also termed the spotted wing drosophila (SWD) or the cherry fly, has achieved the status of one the most important newly emerged insect pests of small soft- skinned fruits (Walsh et al 2011, Asplen et al 2015).
Drosophila suzukiiis a devastating, highly polyphagous fly that is native to Southeast Asia (Asplenet al2015); it was described in 1931 by Matsumura, but this insect was first reported as a pest in 1939 by Kanzawa in Japan (Hauser2011). The damage caused by these insects, however, only gained global attention after almost simultaneous reports of their damage to soft and thin-skinned fruit crops in the USA (Hauser2011) and Europe (many countries) (Grassiet al2009, Calabriaet al2012). Since then, many features of the bioecological roles ofD. suzukiias well as its interactions with the production system have being intensively studied in an attempt to mitigate the economic loses in cultivated crops in North America and Europe [see Asplenet al(2015) for a more complete review].
In contrast to most drosophilid species (Drosophilidae), D. suzukii females have a serrated and strongly sclerotized oviscapt valves that allows them to penetrate the fruit epidermis and lay their eggs inside healthy undamaged fruits (Dreves et al2009, Walsh et al2011, Santos2014, Leeet al2015, Navaet al2015). After the female lays its eggs, over a very short period from 1 to 2 days, the eggs hatch and the larvae start to feed on the fruit tissue (Walsh et al2011). After three molts, the larvae become pupae, from which the adults emerge. At an average temperature of 22°C, this development takes approximately 11 days, followed by 1 to 2 additional days for the adult flies to become sexually mature, copulate, and start laying eggs (Emiljanowicz et al2014, Tochenet al2014, Asplenet al 2015). Hence, in approximately 13–14 days, a new fly gen- eration is laying eggs. The adults can live, on average, up to 70 days, and they show a high reproductive output (Emiljanowiczet al2014).
Thus, due to the high damage potential ofD. suzukiiin addition to the lack of registered pesticides and other reg- ulatory means for controlling the dispersion of these flies in the southern Neotropical region, it is quite interesting to report the seminal efforts already applied to recognize the current status and future perspectives involving this pest in the southern Neotropical region, which herein refers to Uruguay, Argentina, Chile, and the South, Southeast, and Central regions of Brazil. Here, we will present current and future potential damage caused byD. suzukiiin both native and commercial thin-skinned fruits cultivated in the south- ern Neotropical region. Finally, we will also propose future
studies and potential programs to better manage this insect pest in this region.
Current Pest Status in the Southern Neotropical Region
Invasion history and current distribution
In Central and South America, which comprise the majority of the Neotropical region, the first record ofD. suzukiiwas a personal communication (of P. M. O’Grady to M. Ashburner and to J. Máca) of specimens collected in Costa Rica and Ecuador in 1997 and 1998, respectively (Ashburner et al 2005, Calabria et al2012). However, up to the year of 2010, such specimens were not found in any insect collec- tion, and this species had not been recorded again in those countries. Thus, it is difficult to estimate when these flies arrived in the Neotropical regions (Hauser2011). In addition to the inconclusive report described above, it is reasonable to consider the current distribution ofD. suzukiiin the south- ern of the Neotropical region (see Fig1) to have started with invasive infestations that occurred via two possibilities. First, one potential route used to enter the southern Neotropical region refers to the southern region of Brazil, which had the
>75≤100
>25≤50
>50≤75
≤25
known Drosophila suzukii occurrence Probability range as proposed by Benito et al (2016)
Fig 1 Graphical representation of part of the Neotropical region with the known Drosophila suzukii occurrence map overlapping the distribution probability range for this species, as proposed by Benito et al(2016). All plotted dots are based on references listed in Table1, or on the author’s personal observations/unpublished data.
first documented report of this pest in South America (Deprá et al2014). The second possibility, however, points to the Pacific coast of Chile, where the species were collected around Valparaíso port, which imports a variety of fresh fruits from Asia (Medina-Muñozet al2015). To clarify wheth- er these two not mutually exclusive possibilities (or even others) could precisely define the real origin ofD. suzukiiin the southern Neotropical region, it is necessary to conduct genetic and philogeographical analyses. Table1summarizes all the published records of D. suzukii in the southern Neotropical region. Because one the most relevant goals of this forum is to report all existing information about the occurrence ofD. suzukiiand early researches with this pest in the southern Neotropical region, we could not avoid the citation of reports that have only been published in con- gresses or symposium abstract form.
In Brazil, during the first year of the occurrence of D. suzukii(i.e., 2013), the individuals were only collected in traps located in natural reserves (Souza et al 2013, Depráet al2014, Paulaet al2014). TheD. suzukiiindivid- uals were collected in a drosophilid survey using banana- baited traps at a natural reserve in the state of Santa Catarina (SC). Two months later, the same survey program revealedD. suzukiiin the northeast region of the state of Rio Grande do Sul (RS) (Depráet al 2014). Later, during that year,D. suzukii was collected in apple cider vinegar traps placed in a natural forest area in the southern region of RS state (Souzaet al2013). In 2013, oneD. suzukiimale was captured in a banana-baited trap in the central region of Brazil in a natural Cerrado (savannah-like vegetation) reserve at the Brazilian Federal (DF) district (Paula et al 2014). Subsequently, in 2014, D. suzukiiwas reported in agricultural ecosystems, either collected in McPhail traps (Nunes et al 2014) or infesting native cultivated fruits (Müller & Nava2014, Nuneset al2014) in the southern region of RS state. Following these first reports, strawber- ry,Fragaria x ananassaDuchesne (Rosaceae), producers from the northeast of RS state started to experience fruit losses of up to 30% due to infestations by this fly (Santos 2014). The presence ofD. suzukiiin the state of Paraná was also reported by Geisler et al(2015). Collectively, these findings allow us to state thatD. suzukii is currently dis- tributed and well established throughout the entire south- ern region of Brazil (Fig1).
Outside the southern region of Brazil, D. suzukii was reported in 2014 in the São Paulo municipality, São Paulo state (SP), developing in marketed blueberry fruits that were produced in the municipality of São Joaquin, SC state (Vilela & Mori2014). Furthermore,D. suzukiiwas also col- lected in traps placed in a native Atlantic Rainforest in the state of Rio de Janeiro (RJ) (Bitner-Mathéet al2014) and from strawberry fields in the state of Minas Gerais (MG) (Andreazzaet al2016a).
In Uruguay and Argentina,D. suzukiiwas found infesting blueberries, Vaccinium ashei Reade (Ericaceae), and rasp- berries, Rubus idaeus L. (Rosaceae) (Cichón et al2015, Gonzálezet al2015, Santadinoet al2015), but in Uruguay it was also found in traps in the urban area of Montevideo city (Gonzálezet al2015). In Chile, there has only been one report of this species, which was collected from traps near the Valparaiso Port (Medina-Muñozet al2015).
Damage ability and cultivated hosts in the Southern Neotropical Region
Currently, the main cultivated host that is susceptible to se- vere economic losses in the southern Neotropical region is strawberries, which have been shown to achieve production losses up to 30% (Santos2014). However, other common non-native cultivated soft and thin-skinned fruits, such as blueberries, as well as native fruits such as the Surinam cher- ry, Eugenia uniflora L. (Myrtaceae), and Cattley guava, Psidium cattleyanumSabine (Myrtaceae) (Fig2), have been reported under high levels of natural infestations (Müller &
Nava2014, Santadinoet al2015).
The southern Neotropical region exhibits a high over- lap of environmental conditions with the northern hemi- sphere, where D. suzukii is well established (Kenis et al 2016). Hence, many of the crops cultivated in the south- ern Neotropical region are known as hosts of D. suzukii.
This is the case for blackberries [Rubus sp. (Rosaceae)], blueberries, cherries [Prunus cerasus L. (Rosaceae)], grapes [Vitis vinifera L. (Vitaceae)], peaches [Prunus persica (L.) Batsch (Rosaceae)], plums [Prunus domestica L. (Rosaceae)], raspberries, and strawberries. In addition to the similarity of the cultivated hosts, the southern region of Brazil, as well as Uruguay and part of Argentina, has a highly favorable Climex (a common model used to predict the potential geographic distribu- tion of alien pest species), which increases the economic damage potential of this pest (Benitoet al. 2016). These authors observed percentages of overlap between po- tential host cultivation and the highly favorable Climex area they defined forD. suzukii,which ranged from 45.5 to 98.3% for six potential cultivated hosts. The same authors estimated monetary economic loses of US$
21.4 million for peaches and US$ 7.8 million for figs, but they could not estimate losses for the other hosts due to the lack of data.
It is important to note that, at least for some peach culti- vars,D. suzukiidisplays very low oviposition on undamaged fruits but can use damaged fruits as a reservoir host (Andreazzaet al2017a). The same pattern has been observed during infestation of the apple, Malus domestica L.
(Rosaceae), in which prior damage is necessary for D. suzukiioviposition to occur (Oliveiraet al2015).
Table1SummaryofthepublishedreportsofDrosophilasuzukiicollectedfromtrapsorinfestedfruitsinthesouthernNeotropicalregion. Baitedwith/hostNLocationDateReference Traps Banana1NovaVeneza-SC,BrazilFeb2013Depráetal(2014) Banana40Erechim-RS,BrazilMar2013Depráetal(2014) Banana45Botuverá-SC,BrazilApr2013Depráetal(2014) Banana2VilaMaria-RS,BrazilMay2013Depráetal(2014) Banana68Osório-RS,BrazilMay2013Depráetal(2014) Banana1Brasilia-DF,BrazilDec2013Paulaetal(2014) Banana461Torres-RS,BrazilMay-Oct2013Alexandre(2016) BananaUnknownSC,Brazil2013–2014Ramírezetal(2015) Banana25Montevideo,UruguayFeb2014Gonzálezetal(2015) Banana1Brasilia-DF,BrazilApril2014Paulaetal(2014) Banana3Petrópolis-RJ,BrazilNov2014Bitner-Mathéetal(2014) Applecidervinegar21CapãodoLeão-RS,BrazilSep2013Souzaetal(2013) Applecidervinegar21Vacaria-RS,BrazilMar2015Oliveiraetal(2015) ApplecidervinegarUnknownFarroupilha-RS,Brazil2015Borbaetal(2016a) Plum67Valparaiso,Chile2015Medina-Muñozetal(2015) McPhailtrapUnknownMorroRedondo-RS,BrazilNov2013-Feb2014Nunesetal(2014) McPhailtrapUnknownSouthernUruguayMar2014pers.comm.inGonzálezetal(2015) Yellowpantrap17LaRioja,ArgentinaMar2015Lueetal(2017) Miscellaneous13pertrapSãoJoaquim-SC,BrazilJan2016Padilhaetal(2016) Collectedfromfruits Butiasp.2Torres-RS,Brazil2013–2014Alexandre(2016) Eriobotryajaponica(Thunb.)300Pelotas-RS,BrazilSep2014Andreazzaetal(2016b) Eriobotryajaponica(Thunb.)15UniãodaVitória-PR,Brazil2014Geisleretal(2015) EugeniainvolucrataDC.26PortoVitória-PR,Brazil2014Geisleretal(2015) EugeniaunifloraL.116Pelotas-RS,BrazilunknownMüller&Nava(2014) EugeniaunifloraL.67Pelotas-RS,Brazil2014/15cropAndreazzaetal(2015) FragariaxananassaUnknownVacaria-RS,BrazilJan2014Santos(2014) Fragariaxananassa35Ervália-MG,BrazilMar2016Andreazzaetal(2016a) Fragariaxananassa1489Pelotas-RS,Brazil2015/16cropWollmannetal(2016) PrunuspersicaL.3UniãodaVitória-PR,Brazil2014Geisleretal(2015) PrunuspersicaL.UnknownFarroupilha-RS,Brazil2015Borbaetal(2016b) PsidiumcattleianumSabine161CapãodoLeão-RS,BrazilunknownMüller&Nava(2014) PsidiumcattleianumSabine101Cerrito-RS,BrazilunknownMüller&Nava(2014) PsidiumcattleianumSabine36Pelotas-RS,BrazilunknownMüller&Nava(2014) PsidiumcattleianumSabine23Pelotas-RS,Brazil2014/15cropAndreazzaetal(2015) PsidiumguajavaL.UnknownMorroRedondo-RS,BrazilNov2013,Feb2014Nunesetal(2014) PsidiumguajavaL.388Pelotas-RS,Brazil2014/15cropAndreazzaetal(2015) PsidiumguajavaL.3Ervália-MG,BrazilMar2016Andreazzaetal(2016a) RubusidaeusL.UnknownRioNegro,Argentina2014Cichónetal(2015)
Among other factors that might increase or suppress the pest potential of this species in South America is the ability to interact with fruits that have been damaged by other pest species, as is the case for the introduced and well-established African fig fly,Z. indianus(Commaret al2012), and the native South American fruit fly,Anastrepha fraterculus(Wiedemann) (Diptera: Tephritidae) (Malavasi & Zucchi2000). In strawberry fields, drosophilid-like larval damage appears to result in in- creased effects ofZ. indianuscompared withD. suzukii(Nava et al2015, Andreazzaet al2016a).
In a recent survey (2016–2017) in three municipalities of MG state, larger numbers of Z. indianus compared with D. suzukii(12.9 vs 0.2; 4.8 vs 0.0 and 0.2 vs 0.04, flies per fruit) were harvested from strawberry fruits with very low visual damage (author’s unpublished data). The potential in- teractions between these two species have also been established elsewhere (Renkema et al 2013, Fartyal et al.
2014, Joshiet al2014, Lasa & Tadeo2015), highlighting the hypothesis that the co-occurrence of these pest species can increase the damage and economic losses in strawberry pro- duction and potentially other fruit crops. For example, al- thoughZ. indianusis known to be incapable of laying eggs inside healthy undamaged fruits, (Ragaet al2003), a recent investigation has revealed not only the ability ofZ. indianus to infest undamaged strawberry fruits but also the increased infestation ability when the fruits were previously infested by D. suzukii(Bernardiet al2017).
In contrast, the presence ofA. fraterculusmight reduce the damage potential ofD. suzukiiinfestations, or it may not influ- ence theD. suzukiiattack capacity. In a susceptibility screening study using grape cultivars, the presence of oviposition punc- tures or of the development ofA. fraterculuslarvae did not induce D. suzukii oviposition (Andreazza et al 2016c).
Additionally,A. fraterculusintrinsically infests fruits before they reach an advanced ripening stage (Bisogninet al2015), which seems to be the preferable stages for D. suzukiiinfestations (Burracket al2013). Thus, depending on the market fruit des- tination and theA. fraterculusinfestation intensity, it would be sufficient to cause the major economic loses, reducing the im- portance ofD. suzukiiinfestation.
The abilities ofD. suzukiito infest damaged fruits can turn less preferred hosts (e.g., peaches) into highly infested sites (Bellamyet al2013, Andreazzaet al2017a), which might result in more severe infestations in preferred hosts that are cultivat- ed nearby. Consequently, the role of previously damaged or less preferred hosts, as well as the native fruit species, must never be disregarded when considering the management of this pest.
Potential native hosts
As previously reported in Europe and North America (Poyet et al2014, Leeet al2015),D. suzukiican infest many native non-cropping hosts. Countries with continental proportions, Table1(continued). Baitedwith/hostNLocationDateReference RubusidaeusL.4Torres-RS,Brazil2013–2014Alexandre(2016) Rubussp.8630Pelotas-RS,Brazil2015/16cropWollmannetal(2016) VacciniumasheiReade44Canelones,UruguayJan.2014Gonzálezetal(2015) Vacciniumspp.100BuenosAires,ArgentinaDec.2014Santadinoetal(2015) Vacciniumspp.12InterceptedatSãoPaulo-SP,BrazilFeb2014Vilela&Mori(2014) MiscellaneousUnknownSalto,UruguayMay-Mar2014Gonzálezetal(2014) MiscellaneousUnknownSanJosé,UruguayMay-Mar2014Gonzálezetal(2014) MiscellaneousUnknownCanelones,UruguayMay-Mar2014Gonzálezetal(2014) MiscellaneousUnknownMontevideo,UruguayMay-Mar2014Gonzálezetal(2014)
such as Brazil, offer the most varied climate types and plant hosts forD. suzukiiinfestations. Several native (and also exotic) fruits can offer conditions for the development and establish- ment ofD. suzukii, which raise serious concerns about how and when mitigate the losses caused by this pest (Schleseneret al 2014, Schleseneret al2015). Although it is not a native plant of the southern region of Brazil, the Loquat,Eriobotrya japonica (Thumb.) Lindley (Rosaceae), anotherD. suzukiihost (Keniset al 2016) is well established and naturally found among the native vegetation in the south of Brazil. As described in Table1, several recent investigations have demonstrated the ability ofD. suzukii to attack fruit species native to the southern Neotropical region (Müller & Nava2014, Nuneset al2014, Andreazzaet al2015, Geisleret al2015, Souzaet al2017).
Thus, additional studies attempting to investigate the sus- ceptibility of native plant species to the oviposition ofD. suzukii (Table2) are sorely needed. This study will provide a better understanding ofD. suzukiiestablishment in the southern Neotropical region and help to predict geographic isolation due to lack of suitable hosts. Furthermore, knowledge of pos- sible alternative hosts can help to create an annual host calen- dar (as shown in Fig3), which will facilitate temporal predictions of howD. suzukiimigrates from and returns to the surrounding natural or agricultural habitats to the fields.
Management strategies
Since D. suzukii has a very short life cycle, a long adult lifespan and a high reproductive output (Emiljanowiczet al
2014, Tochenet al2014), management strategies must tar- get both immature and adult life stages of this pest. Most of the management programs established forD. suzukiiworld- wide, however, still rely heavily on applications of chemical insecticides (Hayeet al2016), especially in regions with zero tolerance for this pest, such as some states in the USA (Van Timmeren & Isaacs2013). Thus, many research efforts have been conducted to evaluate the efficacy of several commer- cially available insecticides in North America and Europe, which has led to the identification of several chemical groups that provide satisfactory control levels (Beers et al2011, Bruck et al2011, Haviland & Beers 2012, Van Timmeren &
Isaacs2013, Cuthbertsonet al2014). However, despite re- cent investigations showing that some commercially avail- able products in Brazil provide effective control against im- mature and adult life stages of D. suzukii (Andreazzaet al 2017c), none of these products is officially registered by the Brazilian federal control agencies againstD. suzukii (MAPA 2016). Similar situations are observed in Uruguay (MGAP- Servicios Agrícolas 2017) and Chile (SAG 2017). For Argentina, there is still, to our knowledge, no available infor- mation regarding the official registration of synthetic insecti- cides againstD. suzukii.
The lack of registered products has not reduced the use of other management strategies. The use of good agricultural practices (i.e., field sanitization) is the major key for the suc- cess ofD. suzukiimanagement (Navaet al2015, Hayeet al 2016). Since the period from egg to adult is very short, har- vesting fruits over shorter intervals and eliminating
a b
c d
3 mm
1 mm Psidium caleianum Sabine (Caley guava)
Eugenia uniflora L. (Surinam cherry)
Fig 2 Drosophila suzukiidamage in two Neotropical native hosts.
a–bFruit of Cattley guava, Psidium cattleianum.c–dFruit of Surinam Cherry, Eugenia uniflora.
In (a), it is possible to see a D. suzukiilarva on the fruit surface (dotted circle).b,dWhite egg filaments emerging from the oviposition punctures made by D. suzukii(black arrows).
Table 2 Confirmed and potential host plants forDrosophila suzukiiin the southern Neotropical region.
Scientific name Family name Common name
Confirmed exotic cultivated hostsa
Actinidia chinensisPlanch. Actinidiaceae Kiwi
Diospyros kaki Thunberg Ebenaceae Kaki
Eriobotrya japonica(Thunb.) Lindl. Rosaceae Loquat
Ficus caricaL. Moraceae Figs
Fragariax ananassaDuchesne Rosaceae Strawberry
Malus domesticaL. Rosaceae Apple
Morusspp. Moraceae Mulberry
Prunus armeniacaL. Rosaceae Apricot
Prunus aviumL. Rosaceae Sweet cherry
Prunus domesticaL. Rosaceae Common plum
Pyrus communisL. Rosaceae European pear
Pyrus pyrifolia(Burm.) Nak. Rosaceae Asian pear
Rubus fruticosusL. Rosaceae Blackberry
Rubus idaeusL. Rosaceae Raspberry
Vacciniumspp. Ericaceae Blueberries
Vitis labrusca Vitaceae Fox grape
Vitis viniferaL. Vitaceae Grape vine
Confirmed native hostsab
Acca sellowiana(O.Berg) Burret Myrtaceae Feijoa
Butiaspp. Arecaceae Butiá (a type of palm tree)
Eugenia involucrataDC. Myrtaceae Cherry of Rio Grande
Eugenia unifloraL. Myrtaceae Surinam cherry
Prunus serotinaEhrhart Rosaceae Wild black cherry
Psidium cattleianumSabine Myrtaceae Cattley guava
Psidium guajavaL. Myrtaceae Common guava
Potential native hostsb
Allophylus edulis(A St.Hil.) Radlk. Sapindaceae Chal-chal Campomanesia guazumifolia(Camb.) Berg. Myrtaceae Sete-Capotes
Campomanesia phaea(Berg) Landrum Myrtaceae Cambuci
Campomanesia pubescens(Aubl.) Griseb. Myrtaceae Guabiroba
Campomanesia xanthocarpaO. Berg Myrtaceae Guabiroba
Eugenia brasiliensisLam. Myrtaceae Grumixama
Eugenia candolleanaDC. Myrtaceae Cambuí
Eugenia guabijuO.Berg Myrtaceae Guabijú
Eugenia mattosiiD.Legrand Myrtaceae Cereja anã
Eugenia subterminalisDC. Myrtaceae Cambuí-Pitanga
Eugenia uvalhaCambess. Myrtaceae Uvaia
Garcinia gardnerianaMart. Clusiaceae Bacupari
Myrciaria cuspidataBerg in Mart. Myrtaceae Cambuí
Myrciaria glaziovianaKiaersk Myrtaceae Jabuticaba-amarela
Odontocarya acuparataMiers Menispermaceae Capeba
Plinia aureana(Mattos) Myrtaceae Jabuticaba-branca
Plinia cauliflora(Mart.) Kausel Myrtaceae Jabuticaba
Plinia edulis(Vell.) Sobral Myrtaceae Cambucá
The host status was based on: Ciniet al(2012), Bellamyet al(2013), Asplenet al(2015), Leeet al(2015), Keniset al(2016), Souza et al (2017).
a = Preferred host.
bAll hosts are native in south and/or southeast Brazil, and some are native also in Uruguay and Argentina. The authors did not include plant species from Chile in this suggested list.
(destroying) any damaged fruit can partially prevent the de- velopment of new adults in the field. Pruning fruit trees or removing dead leaves from strawberries (Navaet al2015), as well as managing intercropping weeds, promote less favor- able environments for this pest, which prefers a humid mi- crohabitat and a mild temperature (Tochen et al 2014, Tochenet al2016).
One effective, but costly, strategy is the use of netting to cover the plants, preventing the contact of flies with the fruits (Nava et al2015). In some countries in Europe, the use of netting associated with mass trapping and chemical insecticides has been shown to be effective againstD. suzukii (Ioriattiet al2015). In Brazil, where there are currently no quarantine actions or legal tolerance levels to be followed, the growers can legally manage their fields with a low and acceptable population level of the pest.
Finally, the use of biological agents to suppressD. suzukii has also been intensively investigated (Asplenet al 2015).
There are reports of several parasitoids species attacking D. suzukii (Chabert et al 2012, Gabarraet al 2015, Daane et al2016, Guerrieriet al2016), and the application of path- ogens such as nematodes and fungi are part of on-going efforts in many countries (Hayeet al2016). One of the most prospective parasitoid species is Trichopria drosophilae Perkins (Hymenoptera: Diapriidae), which presents high levels of pupal parasitism (Wanget al2016) and could control D. suzukii in strawberry cultivated in greenhouses in Italy (Trottinet al 2014). In the southern Neotropical region, a closely related species, Trichopria anastrephae Lima (Hymenoptera: Diapriidae), and Leptopilina boulardi (Barbotin, Carton & Kelner-Pillault) (Hymenoptera:
Figitidae) were recently reported to attackD. suzukiipupae and larvae in strawberry and blackberry fields (Wollmann
et al 2016). In the same region, T. anastrephaewere also collected from strawberry fruits and mass reared in the lab- oratory on either pupae of D. suzukii or Z. indianus (Andreazzaet al2017b). These previous results are very im- portant and provide a prospective for the development of both conservative and augmentative biological control in the southern Neotropical region.
Future Perspectives
Potential distribution range: observations of Its dispersion paths
The main factor that might limit futureD. suzukiiestablish- ment in Brazil, as well as other parts of the southern Neotropical region, is the combination of adequate temper- ature and relative air humidity (Benito et al 2016). These factors were well discussed in their work, and their results are partially presented in Fig1. Furthermore, the availability of potentialD. suzukiihost plants is a relevant factor capable of impacting the distribution ofD. suzukiiin the Neotropical region. As shown in Table2, several plant species can serve as potential hosts forD. suzukii. However, knowing that this species is highly polyphagous (Keniset al2016), we should expect a lack of some other potential hosts that are not listed in this table that can also expand the limits of the distribution and establishment ofD. suzukii.
The application of adequate laws to regulate the fresh fruit trade market, not only among the regions proposed by Benitoet al(2016), might be the most effective way to delay the arrival and establishment ofD. suzukiiin new areas.
Some important considerations concerning the invasion
Winter Spring Summer Fall
Surinam cherry Strawberry Peach Blackberry Plum Blueberry Raspberry Fig Grape
Loquat
Ca y guava ated hosts
Alterna e hosts
July August September October November December January February March April May June
Fig 3 Proposed annual calendar showing the availability ofDrosophila suzukiihosts in suitable stage (bars) (ripe fruits-near harvest) in the macro- region of Pelotas-RS, Brazil. The host phenology was based on: Bianchiet al(1998), Raseiraet al(2004), Antuneset al(2008), Castro (2008), Madail &
Raseira (2008), Azambuja (2009), Azevedo (2010), Cardosoet al(2012), Carvalho (2013), Bisogninet al(2015). See Table2for the host’s scientific names.
history in the southern Neotropical region, as described ear- lier in the text, are helpful to understand the rapid spread of D.suzukiiin this region.
In the same year thatD. suzukiiwas first recorded in the south of Brazil (Depráet al2014), the species was also re- ported in a natural reserve approximately 1400 km north of that locality (Paulaet al 2014). Although further investiga- tions are needed to evaluate whether the single specimen collected in this second location is or is not related to the first ones, these two consecutive reports suggest the rapid dis- persion capacity ofD. suzukii. The infestation in Uruguay and Argentina are likely a consequence of the natural spread of this species after its introduction in the southernmost region of Brazil, especially due to the geographical proximity and absence of physical barriers. However, the hypothesis that the introduction of D. suzukii to these countries (i.e., Argentina and Uruguay) occurred through the fresh fruit trade market, either from Brazil or from other infested re- gions such as North America, Europe, or Asia, cannot be overlooked. This last hypothesis is strongly applicable to the case in Chile, where the fly was found only in traps near Valparaíso Port in Valparaiso city, which imports large amounts of fresh fruits, such as plums, from Asia (Medina- Muñoz et al2015). These authors also highlighted that D. suzukiispecimens present in this region of Chile had a strong preference for plum-baited traps instead of banana- baited traps, supporting the close relationship with this host.
The dispersion path through the fresh fruit trade market was also reported in Brazil in 2014, when blueberries grown in SC state hadD. suzukiiinfestations at a fruit market in São Paulo city (Vilela Mori 2014). Another host that certainly provided means for the dispersion of this pest is the grape.
In January 2017, a large number ofD. suzukiiflies were ob- served and collected in grapes being transported to a winery on a truck approximately 90 km from its growing location in R S s ta te , B ra z il ( a u th o r’s pe rso na l o bser vatio n ).
Independently if the flies were the primary or secondary organisms infesting these grapes, according to the driver, a delivery of grapes from the same field would be performed the next day in a winery in SC state, which is approximately 250 km from the growing field. Even the Brazilian Ministry of Livestock and Supply is monitoring the presence of the spe- cies in some production regions (not in all states) (authors’ personal information), the lack of further information about the presence of the pest and mitigation of regulatory means clearly contribute to the actual scenario of D. suzukii invasion.
Corroborating the predictions of Benitoet al(2016), dos Santoset al(2017), based on climatic variables, mathemati- cally predicted that the central region of southern Brazil, the southern half of Paraguay, all of Uruguay, and the east and south of Argentina are potential distribution areas for D. suzukii. On the Pacific coast, the entire coastline of Chile
is indicated as a potential distribution area of this insect pest.
The areas of greatest environmental suitability forD. suzukii are in southern Chile, Uruguay, on the south coast and in south Brazil, and along a small range on the northern coast of Argentina (dos Santoset al2017).
What to do to mitigate the problem
According to current knowledge aboutD. suzukiibioecology in areas where this pest is already established (Asplenet al 2015), as well as the similarities of its interactions with hosts that have been damaged by some other well-known fruit fly pests (Diptera: Tephritidae), it is necessary to consider area- wide (AW) integrated pest management (IPM) programs.
The AW approach has also recently been recommended by research conducted in the Northern Hemisphere (Ciniet al 2012, Asplenet al2015, Hayeet al2016, Keniset al2016). The best way to cope with this pest is a well-integrated compos- ite of actions by regulatory agencies, researchers, extension services, and growers, which can be a great challenge in some parts of the southern Neotropical region due to the cultural characteristics and historical experience of growers in terms of managing other native fruit fly species.
Unfortunately,D. suzukiihas never been included in any quarantine list in Brazil (the authors have no information about Uruguay, Argentina and Chile), which would have alerted customs barriers and extension services to readily establish monitoring programs in the most susceptible areas, near ports and in areas with potential host plants.
Nevertheless, regulatory actions are still needed and are very useful, especially to avoid continued reintroductions (Cini et al2014) that could increase, for example, the source of insecticide resistance genes. Controlling fresh fruit trade market is essential since it has been suggested to be the main dispersion means of this pest worldwide (Ciniet al2014) as well as in the southern Neotropical region (Vilela & Mori 2014, Medina-Muñozet al2015).
Another important action to be taken by the regulatory agencies and industries is the registration of insecticides and biological control agents for safe and legal use in the field.
The lack of registered control agents can lead to an increase in the unregulated and illegal market of pesticides as well as its unsafe use in the field. In this respect, laboratory and field efficacy screening tests with products that have already been registered to manage other pests in D. suzukii cultivated hosts are sorely needed, which can reduce the amount of paperwork and time needed to obtain the product licenses.
Some information regarding the synthetic insecticides used in Brazil is already available (Andreazzaet al2017c), but ad- ditional studies are still needed.
In addition to regulatory actions, the extension service must gather as much information as possible on the available D. suzukiimanagement strategies [as in Navaet al(2015) and
Hayeet al(2016)] and work with the growers to delay this pest establishment in production fields. As discussed above, one of the main bottlenecks for the implementation of an AW-IPM forD. suzukiiin the southern Neotropical region is the knowledge about the host suitability of native or non- cultivated fruit plants, as reported by Diepenbrock et al (2016) and Keniset al(2016). Finally, more field surveys for endemic parasitoid species, such as that conducted by Wollmannet al(2016), and the development of mass rearing techniques for these parasitoids (Andreazzaet al2017b) will support information to plan conservative and augmentative biological control programs in each macroregion of the southern Neotropical region.
In addition to the most common or traditional manage- ments approaches, studies must also focus on products and strategies that cope with organic production regulations in each country or meet international market reduction of res- idue requirements, as described by Haviland & Beers (2012).
Screening for non-synthetic insecticides (e.g., plant extracts, essential oils, or other products already used by local organic growers that may be effective against this species) will pro- vide alternative options that could be integrated with the other management practices discussed earlier in the text.
Growers are a key piece for the sustainable management of this pest. All the management strategies discussed herein and in other studies [such as in Ciniet al(2012), Asplenet al (2015), Nava et al(2015) and Hayeet al(2016)] should be applied by growers with professional supervision, especially if an AW-IPM program should be ever applied. Some recom- mendations, such as the destruction or sanitization of any other fruit species around the production field, may experi- ence barriers in farm borders when neighborhoods refuse to participate in AW management of this pest, or if native protected vegetation areas are located nearby. Thus, a reg- ulatory disposition coordinating these actions is necessary.
Development of a large-scale (AW-IPM) management program forD. suzukii
The concept of the AW approach for pest management was introduced by Knipling and Rower (Kogan1998). However, even before its conceptualization, the AW approach was al- ready used against several invasive pests [e.g., the grafting of all European grapes with American phylloxera-resistant root- stocks; the eradication of the tsetse fly Glossina palpalis Robineau-Desvoiy (Diptera: Glossinidae) from Portugal in 1914; and the fruit fly management programs in the USA, as reported for Ceratitis capitata Wiedemann (Diptera:
Tephritidae) in California] (Vreysen et al 2007). In theory, the AW approach must be applied over large geographical areas led by organizations rather than by individual farmers, with a focus on population suppression or, if viable, eradica- tion of the pest (Kogan 1998).Drosophila suzukii possesses
bioecological characteristics, such as its high polyphagia, that compromise any eradication programs for this species in re- gions with high host availability and climate adequacy for the species. Hence, population suppression should be the focus of a management programs in the southern Neotropical re- gion (perhaps in Chile, geographical isolation might be con- sidered), and an AW approach using IPM strategies is likely optimal. However, it is important to note the social concerns about the strategies employed, the willingness of the farmers to collaborate, and the lack of regulatory efforts to prevent consecutive re-invasion of the managed regions, represents high threats associated with any AW-IPM program (Vreysen et al2007). These factors partially determine the success or failure of these programs (please see Klassen (2005) for a list of examples). Consequently, regulatory provisions from gov- ernmental agencies coordinating actions, such as the remov- al of alternative hosts from the proximities of the cropping fields, are essential (Vreysenet al2007).
Below, we provide a draft proposal of step-by-step actions to be taken to develop an AW-IPM program to suppress the D. suzukiipopulation not only farm-by-farm but in a wide area, following the proposal by Vreysenet al(2007).
Basic research.The core of any AW-IPM program is the de- velopment of new tools and technologies. According to Vreysen et al (2007), successful programs were achieved when an independent institution was responsible for plan- ning and developing the new tools and methods for the program. Failure in this first step, although it is not noticed during this first program phase, will compromise the entire program.
As a very first point, it is important to understand the genetic“blue print” of the pest species,D. suzukii, within the regions the AW-IPM program to be applied. For this purpose, molecular tools are available (Hoy2013) and make it possible to analyze the genetic diversity and prevent future control failures as a result of this diversity. In association, it is important to access the differential responses of local pest populations to xenobiotics such as insecticides, elucidating and preventing any possible resistance selection. Other tech- niques that might be developed for use in an AW-IPM pro- gram for D. suzukiiinvolve the reduction of reproduction, either by using sterile insect techniques (Klassen 2005), as is currently being used for mosquito control in Piracicaba city, SP, Brazil (Waltz2016), or by usingWolbachia strains that would cause cytoplasmic incompatibility, as is being devel- oped forBemisia tabaciGennadius (Hemiptera: Aleyrodidae) (Zhou & Li2016).
As advocated by the IPM component of the program, other components must be used in association to achieve a successful program (Kogan1998). The study of the local bio- diversity and development of mass rearing techniques for use in augmentative biological programs with endemic
promising parasitoids species is fundamental (Wollmannet al 2016, Andreazzaet al2017b). Additionally, the conservation of this species in the field should be considered, leading to the need for selectivity studies of products that could be used againstD. suzukii.
Modeling and developing new methods.Modeling tools can be used to understand population fluctuations in time and space and to predict the potential pest distribution and/or spreading capacity (Vreysenet al2007). For example, Benito et al(2016) and dos Santos et al (2017) used the climatic index (Climex) and algorithms, respectively, to predict the potential spread ofD. suzukii in the southern Neotropical region. In addition to modeling, the development of new simple tools, such as a year-round calendar of available hosts, strongly helps to coordinate the management efforts over time. This calendar also helps researchers or pest advi- sors to identify gaps or bottlenecks in host availability that may be used to develop new management strategies. Thus, we proposed an annual calendar (Fig3) comprising the knownD. suzukiimain hosts cultivated in the southernmost region of Brazil. Due to the large area of the southern Neotropical region and different production models, the pro- duction calendar greatly varied from and should be adapted into each macro region and updated with information pro- vided from future studies conducted in each location.
Feasibility studies and regulation.In addition to the develop- ment of new tools and technologies by basic research, collecting data for cost/benefit analyses will be fundamental for the success of the WA–IPM program (Vreysenet al2007).
Among these investigations, the continuous collection of da- ta regardingD. suzukiifluctuations throughout the year in fields and natural habitats, as well as the estimation of all possible economic losses caused by these fly infestations, is noteworthy. With these data, feasibility studies can better plan and later monitor the efficiency of the program.
Additionally, the development of a logistical design of culti- vation and IPM component rotation based on both the crop phenology and the pest life-history traits (such as the early proposed crop calendar) is also essential, and a pilot study may be used (Vreysenet al2007).
Well-conducted feasibility studies will help to convince all stakeholders about the program needs, requirements and fund raising. It will also identify logistical challenges such as the availability of resources and infrastructure for an opera- tional program, enabling planning to mitigate all these chal- lenges. Thus, political and regulatory efforts by governmental agencies are necessary (Hendrichset al2007).
The regulatory framework of products and technologies to be used in a potentialD. suzukiiAW-IPM program will aid not only the operability of the program but also the interna- tional trade market. Recently, the first patent deposit of
flavoring esters forD. suzukiicontrol in the Neotropical re- gion represents an example of non-toxic environmentally friendly products being regulated in the southern Neotropical region (Garcia et al 2016). The development and regulation of postharvest treatments that guaranty pest-free products, such as ionizing radiation, which meets International Plant Protection Conventions provisions, will provide additional tools to prevent continuous re- infestations ofD. suzukiiin managed areas.
Pilot and operational AW-IPM programs.The pilot trials are very effective for identifying program failures and improve- ment needs for a completely operational AW-IPM program to be successfully implemented. Thus, in addition to testing technologies commonly used in field-by-field IPM, the testing of technologies more related to the AW approach will be required (e.g., pilot mass-rearing facilities of sterile flies, and/or parasitoids, pilot field release of such species, inten- sive training of staff to work in these facilities). An example is the program that is already being developed in the south of Brazil to rear and mass release sterile fruit fly species and parasitoids (Embrapa2016).
After all the technologies have been tested and validated under field pilot conditions, the program can be implement- ed. Great attention must be used in this phase due to the use of a large-scale area and resources. The political, regulatory and commitment off all parts is essential to guarantee suc- cess. One remarkable recent example of an operational AW- IPM program that does not rely on mass rearing and release of insects (which can be the most challenging part of devel- oping and implementing an AW-IPM program) is the eradi- cation of the boll weevil in the USA. This program has been very successful and is based mostly on intensive monitoring and detection tools, integrated with a few other control tools (Hendrichset al2007), and it serves as an example that with the commitment of all parts (from research, government, growers, industries and market), a fully operational AW- IPM program forD. suzukiiwill be viable in the future.
Final Considerations
The current panorama ofD. suzukiiinfestation in the south- ern Neotropical region is still underinvestigated. Most empir- ical studies (published studies, excluding notes of occur- rence) were developed only in Brazil by a few research groups in an attempt to validate international information for local realities, demonstrating a delay in actions against this alien pest invasion. As discussed in this forum, intensive and integrative studies, such as i—monitoring the pest pres- ence and field fluctuations, ii—identifying and classifying the host status of cultivated and non-cultivated fruit species, iii— identifying and improving any source of natural in-field
biological control, and finally iv—discussing, testing, and de- veloping new tools and management strategies to cope with this highly mobile pest species using an AW-IPM approach system are essential and needed. The integration of the re- search community with growers, especially the collaboration of the governmental regulating agencies for the establish- ment of a collaborative regulatory framework, and the full commitment of funding agencies in providing the necessary resources for the development of science related to this highly damaging invasive species will mitigate economic losses and generate positive profit for the national and inter- national economies of the affected countries.
A large amount of very diverse information was discussed in this forum. The authors hope that their goal of raising the attention of all stakeholders regarding the urgent needs of a cooperative discussion aboutD. suzukiiinvasion has been accomplished. It is very important to search for answers about what can be done to mitigate this problem in an effi- cient, low-cost, environmentally friendly and sustainable way. Thus, we advocate that government and industry should focus more attention on collaborative efforts, such as the promotion of regional, national and international meetings involving the various interested parts.
Acknowledgements Grants from the CAPES Foundation, the National Council of Scientific and Technological Development (CNPq), the Minas Gerais State Foundation for Research Aid (FAPEMIG), and the Empresa Brasileira de Pesquisa Agropecuaria (EMBRAPA) supported this work.
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